Immune cell migration and its functional changes in the peritoneal cavity of mice infected with Echinococcus multilocular

doi:10.12140/j.issn.1000-7423.2025.01.012

CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES ›› 2025, Vol. 43 ›› Issue (1): 76-83.doi: 10.12140/j.issn.1000-7423.2025.01.012

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Immune cell migration and its functional changes in the peritoneal cavity of mice infected with Echinococcus multilocular

DENG Bingqing¹^,²(), ADILAI Duolikun¹^,², LI Yinshi¹^,², ABIDAN Ainiwaer¹^,², SUN Sheng¹^,², XIAO Wenying¹^,², GE Conghui¹^,², TANG Na¹^,², JIANG Tao³, WANG Hui¹^,², ZHANG Chuanshan¹^,², LI Jing¹^,⁴^,⁵^,^*()

1 College of Basic Medical, Xinjiang Medical University, Urumqi 830054, Xinjiang, China
2 Clinical Medicine Research Institute, the First Afilicated Hospital of Xinjiang Medical University, Urumqi 830054, Xinjiang, China
3 Xinjiang Medical University Laboratory Animal Center, Urumqi 830011, Xinjiang, China
4 Key Laboratory of High Incidence Disease Research in Xingjiang (Xinjiang Medical University), Ministry of Education, Urumqi 830054, Xinjiang, China
5 National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research); NHC Key Laboratory of Parasite and Vector Biology (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention), Shanghai 200025, China

Received:2024-10-21 Revised:2025-01-24 Online:2025-02-28 Published:2025-03-26
Contact: *E-mail: lijing0527@163.com E-mail:Bingqingdeng@163.com;lijing0527@163.com
Supported by:
Natural Science Foundation of Xinjiang Uyghur Autonomous Region(2022D01E51);Natural Science Foundation of Xinjiang Uyghur Autonomous Region(2022D01D60);National Natural Science Foundation of China(82302561);National Natural Science Foundation of China(82372279);National Natural Science Foundation of China(82160396);Funding of Open Subjects in the Key Laboratory of the Ministry of Education for the Study of Highly Prevalent Diseases in the Xinjiang Region(2023B03);Provincial-Ministerial Joint Establishment of State Key Laboratory of Causes and Prevention of High Morbidity in Central Asia(SKL-HIDCA-2024-25);Open Topic Funding Program of the Key Laboratory of Parasitic Pathogen and Vector Biology of the National Health Commission of China(NHCKFKT2022-05)

Abstract

Abstract:

Objective To understand the changes in the migration and differentiation of immune cells in the peritoneal cavity of mice infected with Echinococcus multilocularis, and to explore the mechanism of immune function. Methods Spleen tissues of enhanced green fluorescent protein (EGFP) mice were lysed to isolate EGFP-labeled immune cells. C57BL/6J mice were intraperitoneally injected with 2.5 × 10⁷ traced immune cells. Five days later, 3 000 protoscoleces of E. multilocularis were inoculated via the hepatic portal vein. After 19 weeks of infection, the liver and spleen tissues of the infected mice were collected. After frozen sectioning, the sections were stained with 4,6-diamidino-2-phenylindole (DAPI), and immunofluorescence was used to observe the distribution of the traced immune cells. Immune cells from peripheral blood, liver, spleen and peritoneal cavity of infected mice were isolated, and the migration distribution and cell typing of EGFP-labeled immune cells in different tissues were detected by flow cytometry, as well as the secretion of cytokines interferon-γ (IFN-γ), tumor necrosis factor-α (TNF-α) and interleukin-4 (IL-4). Results The immunofluorescence results showed that the EGFP-traced cells mainly migrated to the spleen tissue of the mice. In the liver tissue, the proportions of various types of traced lymphocytes from high to low were as follows: CD8⁺ T cells (79.63 ± 5.00)%, CD4⁺ T cells (7.08 ± 4.00)%, and B cells (2.01 ± 1.00)% (F = 396.20, P < 0.01). In the spleen tissue, the proportions of various types of lymphocytes from high to low were as follows: CD8⁺ T cells (73.97 ± 3.56)%, CD4⁺ T cells (11.92 ± 5.02)% and B cells (3.86 ± 0.32)% (F = 349.00, P < 0.01). In the peritoneal cavity, the proportions of various types of lymphocytes from high to low were as follows: CD8⁺ T cells (45.27 ± 4.53)%, CD4⁺ T cells (34.60 ± 8.00)% and B cells (15.03 ± 6.38)% (F = 16.90, P < 0.05). The numbers of traced CD4⁺ T cells in the liver, spleen, and peritoneal cavity were 2 700 ± 3 120, 14 407 ± 11 958 and 3 376 ± 1 481 respectively. The numbers of traced CD8⁺ T cells were 26 407 ± 22 190, 109 179 ± 92 692 and 4 245 ± 798 respectively. The numbers of traced B cells were 698 ± 719, 5 794 ± 4 971 and 1 476 ± 840 respectively. All three types of traced lymphocytes were mainly distributed in the spleen tissue (F = 2.51, 3.03, 2.62, all P > 0.05). In the liver tissue, the proportions of various types of myeloid cells from high to low were as follows: dendritic cells (3.94 ± 1.33)%, monocytes (3.79 ± 1.80)%, macrophages (3.13 ± 1.85)%, eosinophils (2.40 ± 1.81)%, myeloid-derived suppressor cells (0.76 ± 0.17)% and neutrophils (0.67 ± 0.04)% (F = 3.21, P < 0.05). In the spleen tissue, the proportions of various types of myeloid cells from high to low were as follows: dendritic cells (1.86 ± 0.89)%, monocytes (0.41 ± 0.09)%, macrophages (0.23 ± 0.03)%, neutrophils and myeloid-derived suppressor cells [both (0.13 ± 0.14)%], and eosinophils (0.04 ± 0.04)% (F = 42.70, P < 0.01). In the peripheral blood, the proportions of various types of myeloid cells from high to low were as follows: dendritic cells (0.37 ± 0.28)%, monocytes (0.22 ± 0.27)%, macrophages (0.22 ± 0.21)%, neutrophils and myeloid-derived suppressor cells [both (0.17 ± 0.08)%], and eosinophils (0.05 ± 0.08)% (F = 0.92, P > 0.05). Among the traced CD4⁺ T cells in the liver tissue, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (41.17 ± 19.92)%, (30.70 ± 3.35)%, and (2.78 ± 4.81)% respectively (F = 8.22, P < 0.05). Among the traced CD8⁺ T cells, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (64.17 ± 3.17)%, (24.85 ± 15.66)%, and (5.67 ± 6.35)% respectively (F = 27.08, P < 0.01). Among the traced CD4⁺ T cells in the spleen tissue, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (52.43 ± 19.43)%, (27.67 ± 18.99)%, and (4.77 ± 2.23)% respectively (F = 6.88, P < 0.05). Among the traced CD8⁺ T cells, the cells secreting TNF-α, IFN-γ, and IL-4 accounted for (40.53 ± 17.79)%, (38.97 ± 18.04)%, and (3.23 ± 3.09)% respectively (F = 6.15, P < 0.05). Among the traced CD4⁺ T cells in the peritoneal cavity, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (64.33 ± 6.82)%, (46.43 ± 13.44)%, and (4.03 ± 3.51)% respectively (F = 36.04, P < 0.01). Among the traced CD8⁺ T cells, the cells secreting IFN-γ, TNF-α, and IL-4 accounted for (53.57 ± 19.17)%, (21.47 ± 8.54)%, and (6.13 ± 8.63)% respectively (F = 10.24, P < 0.05). Conclusion Immune cells in the peritoneal cavity of E. multilocularis infected mice mainly migrate to the spleen tissue, and the cell types are mainly CD8⁺ T cells and dendritic cells. T cells mainly secreted IFN-γ, which showed Th1 immune response.

Key words: Alveolar echinococcoisis, Peritoneal cavity, Immume cell, Migration, CD8⁺ T cell

CLC Number:

R532.32

DENG Bingqing, ADILAI Duolikun, LI Yinshi, ABIDAN Ainiwaer, SUN Sheng, XIAO Wenying, GE Conghui, TANG Na, JIANG Tao, WANG Hui, ZHANG Chuanshan, LI Jing. Immune cell migration and its functional changes in the peritoneal cavity of mice infected with Echinococcus multilocular[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2025, 43(1): 76-83.

Figures/Tables 4

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Immune cell migration and its functional changes in the peritoneal cavity of mice infected with Echinococcus multilocular

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